Seasonal hormones, female reproductive tract changes, and some field observations on breeding activities of the small Indian mongoose (Herpestes javanicus) from its native
range of Potohar Plateau, Pakistan
Faraz AKRIM1, Hira FATIMA1, Saida Amna NAZIR1, Tariq MAHMOOD1, Riaz HUSSAIN1, Muhammad Sajid NADEEM2,*1Department of Wildlife Management, PMAS-Arid Agriculture University Rawalpindi, Rawalpindi, Pakistan
2Department of Zoology, PMAS-Arid Agriculture University Rawalpindi, Rawalpindi, Pakistan
1. IntroductionThe small Indian mongoose Herpestes javanicus (Geoffroy, 1818) is an important small carnivore, especially in agroecosystems where it serves as a biological control agent for snakes, rodents, and insects. The species has a native range in the southern and southeastern regions of Asia (Wozencraft, 2005), from Pakistan and northern India to southern China and the Malay Peninsula, as well as Hainan and Java; in the west, it extends to southern Iran (Corbet and Hill, 1992) and southwestern Afghanistan, along the shore of the Persian Gulf up to Kuwait and Iraq (Hassinger, 1968). In Pakistan, it is widely distributed in 3 out of 4 provinces including the Potohar Plateau and the Salt Range in Punjab Province; however, it has not yet been reported from the province of Khyber Pakhtunkhawa (Roberts, 1997).
Reproduction is a very important phenomenon for survival of an organism, vital for continuation of its generations. Animals reproduce during different times of the year; the timing can be affected by temperature or day length, as well as availability of food for young ones. Many of them breed once a year, while the rest may breed many
times in a year. Previously published studies on introduced island populations of the small Indian mongoose indicate that it can breed 2 to 3 times a year, and breeding is most frequent when food is abundant. Females become sexually mature at 10 months of age and males at 4 months (de Magalhaes and Costa, 2009). Maximum frequency of pregnancies occurs just prior to the summer solstice both north (Pearson and Baldwin, 1953; Nellis and Everard, 1983) and south of the equator. In captive females, the onset of estrus is demonstrated by restlessness and increased marking. Many males may be in attendance to 1 female in estrus. Barking, screaming, and chasing among the males are common at this stage (Nellis and Everard, 1983).
The gestation period lasts for about 7 weeks (49 days) and litters of 3 young ones per female are produced (Pocock, 1941). Hoffmann et al. (1984) studied seasonal reproduction in Herpestes auropunctatus females in Hawaii; during gestation and lactation, no significant changes in body weight were observed. However, levels of LH and FSH were higher in the breeding season compared to the nonbreeding season. Pearson and Baldwin (1953)
Abstract: The small Indian mongoose acts as a biological control agent for rodents, snakes, and many insects in agroecosystems. Its reproductive physiology has been studied mostly from its introduced range. We investigated the reproductive pattern of the female small Indian mongoose on the Potohar Plateau, i.e. its native range. We found a male:female ratio of 0.67 (n = 52); only 16% of the live-trapped females were found to be pregnant. Elevated estradiol and progesterone levels were found during March to May. LH levels showed 2 peaks: the first during March (25.5 mIU/mL) and the second in September (29.8 mIU/mL); however, FSH levels were almost the same. Light microscopic sections (H & E stained) of the ovary showed mature Graafian follicles during February, corpora lutea (early gestation) during March, and maintenance of prominent corpora lutea inside the ovary during April (late gestation period); however, during June, no corpora lutea were observed in the ovary, indicating the lactational phase. Average litter size was 2.83 ± 0.14 (by visual observation), 3 ± 0.24 (by counts of placental scars), and 3.2 ± 0.37 (by counts of developing embryos). The study concludes that the small Indian mongoose breeds twice a year in its native range.
Key words: Reproduction, hormones, histology, ovary, litter size, breeding season
Received: 04.12.2015 Accepted/Published Online: 22.12.2016 Final Version: 17.07.2017
Research Article
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analyzed Herpestes javanicus ovaries at various times during the period of lactation, and found no corpora lutea or ripe follicles, while lactating females had follicles as large as 0.9 mm.
Most of the studies conducted so far on reproductive aspects of the small Indian mongoose have involved introduced populations of the species, on different islands like the Fiji islands (Gorman, 1976), Grenada (Nellis and Everard, 1983), Hawaii (Hoffmann et al., 1984), and Okinawa (Ogura et al., 2001) Island of Japan. However, studies focusing on the species in its native range are scarce. One recent report was on male reproductive hormonal patterns and histological changes in the testes of the small Indian mongoose (Mahmood et al., 2015) of the Potohar region of Pakistan. The current study focused on the reproductive patterns of the female small Indian mongoose, i.e., hormonal (estradiol, progesterone, FSH, and LH) and histological changes in the ovaries during different months of the year, in their native range of the Potohar Plateau.
2. Materials and methodsThe current study was conducted in the Potohar Plateau (32°33′–34°3′N, 71°89′–73°37′E), consisting of an area of 2.2 million hectares (Bhutta, 1999), with an elevation ranging from 305 to 610 m a.s.l. The climate is semiarid to subhumid; maximum temperature reaches 45 °C during summer, but in winter it decreases below freezing point (Encyclopedia Britannica, 2010).2.1. Live trappingIn the study area, potential sampling sites and mongoose populations (as well as their burrows) were identified. Individuals were marked using plastic wires of different colors. Females were live-trapped using specially designed mesh traps to record observations on their state of pregnancy; 6 traps were used at each trapping session. The traps were set, depending upon the abundance of the active burrows of the species, at appropriate places at midday or in the evening, and then checked the next dawn. Traps were checked regularly during the active time for mongooses (from 1000 to 1600). Poultry waste was utilized as bait in the traps to attract the animals. Trapped male individuals were released back to the same habitat. Most of the female individuals were also released after recording the data; however, for histological studies, some individuals were sacrificed.2.2. Field observationsPhysical observations of the bellies of captured females were made to confirm the state of pregnancy. To establish the sex ratio (M:F) in the population, the sex of live-trapped animals was identified and established by observation of their external genitalia. Field observations were also taken on mating behavior during the breeding season,
and the records were maintained for subsequent analysis. Footprints were observed around the burrow openings to confirm burrow occupancy during the breeding season. The length of the gestation period was assessed by maintaining records of observations taken from the day of mating until the birth of the pups. 2.3. Hormonal estimationsFor investigating hormonal concentrations and ovarian changes, some of the trapped females were euthanized with chloroform and sacrificed to collect blood and ovary tissue samples. All animal handling and sacrifice were carried out in accordance with the guidelines provided by the University (PMAS-AAUR/2646), and approved by the Ethical Committee (dated 30 April 2012). Blood was drawn directly from the heart by cardiac puncture in EDTA-containing tubes, centrifuged at 3500 rpm for 15 min to obtain plasma, and stored at –20 °C until final analysis. The stored plasma samples were processed for estimation of 2 gonadal hormones, estrogen and progesterone, and 2 gonadotropins, FSH and LH, by using commercially available ELISA kits (Amgenix, USA).2.4. Light microscopyThe ovarian tissues were weighed and fixed in 10% formalin, and processed for standard histological procedures; 5–7-µm tissue sections were cut and stained with hematoxylin and eosin (H & E) for light microscopic study. The sample size was N = 20, which included 2 samples each for 7 months (i.e. March–December), while the remaining 5 months of the year had 1 sample each.2.5. Litter sizeLitter size was determined using 3 different approaches: first, by physical observations of the number of pups accompanying their parents seen for the first time in the field during daily activity; second, by counts of embryos inside the uterus obtained by dissecting pregnant females; and third, by counts of placental scars (found after females had given birth).
3. Results3.1. Body measurementsAverage body length of adult females was 51.6 ± 0.58 cm; the average body weight was found to be 368.75 ± 17.48 g (Table 1). 3.2. Sex ratioA total of 52 individuals of the small Indian mongoose were trapped from Jabairpur (N = 14), Choa Saiden Shah (N = 15), Nakka Kahout (N = 03), Kallar Kahar (N = 09), and Danda Shah Bilawal (N = 11). Among those, 21 were male and 31 were female, giving a sex ratio of M:F = 0.67 (Table 2). Of all females that were captured, only 16% (5) were pregnant.
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3.3. Hormonal concentrationsEstradiol levels started elevating in February 2013 (233 pg/mL) and increased during March (782.55 pg/mL), April (765.9 pg/mL), and May 2013 (856.3 pg/mL). Lower levels were noted (Table 3) after this time, although
samples from August to February were also adult (Figure 1). Progesterone levels (Figure 2) also started rising from February 2013 (8.48 ng/mL) onwards, and were elevated during March (15.6 ng/mL), April (13.9 ng/mL), and May 2013 (12.1 ng/mL). The highest FSH levels (Figure 2) were
Table 1. Body measurements of female small Indian mongoose (Herpestes javanicus) from the Potohar Plateau from July 2012 to June 2013.
Month Capture site GPS location Reproductive status
Body length (cm)
Body weight (g)
July 2012AAUR Fields Rawalpindi
N33°36′21.1″E073°02′38.5″Elevation: 502 m a.s.l. Lactating 53.34 371
August 2012 Graveyard Seham Road Rawalpindi
N33°36′21.8″E073°02′37.4″Elevation: 502 m a.s.l. _
52.84 334
September 2012 Graveyard Seham Road Rawalpindi
N33°36′21.8″E073°02′37.4″Elevation: 502 m a.s.l.
_ 53.34 354
October 2012 Dhoke Fateh AttockN33° 31′25.4″E072°38′37.5″Elevation: 488 m a.s.l. _
51.82 325
November 2012 Dhoke Fateh Attock
N33°31′25.4″E072°38′37.5″Elevation: 488 m a.s.l. _
53.34 362
December 2012 Chakri Road Rawalpindi
N33°32′49.8″E072°54′57.6″Elevation: 473 m a.s.l. _
49.53 359
January 2013Harley Street Rawalpindi
N33°34′33.5″E073°02′41.8″Elevation: 497 m a.s.l. _
48.26 242
February 2013Harley StreetRawalpindi
N33°34′33.5″E073°02′41.8″Elevation: 497 m a.s.l. _
53.34 350
March 2013 Lalkurti RawalpindiN33°34′48.2″E073°03′24.3″Elevation: 508 m a.s.l.
Pregnant 51.82 472
April 2013 Lalkurti RawalpindiN33° 34′48.2″E073°03′24.3″Elevation: 508 m a.s.l.
Pregnant 53.34 453
May 2013Harley Street Rawalpindi
N33° 34′33.5″E073°02′41.8″Elevation: 497 m a.s.l.
Pregnant 49.53 418
June 2013DhairiHassanabad Rawalpindi
N33°54′02.7″E072°45′52.08″Elevation: 433 m a.s.l.
Lactating 48.77 385
Mean 12 sites 51.6 ± 0.58 368.75 ± 17.48
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recorded during July 2012 (1.47 mIU/mL), August 2012 (1.39 mIU/mL), and September 2012 (1.37 mIU/mL). LH levels showed 2 peaks: the first during September 2012 (29.8 mIU/mL) and the second during March 2013 (25.5 mIU/mL) (Figure 2).3.4. Histological findingsIn general, females captured during March, April, and May 2013 were pregnant, while those captured in June and July were lactating. Hematoxylin and eosin-stained light microscopic sections of the ovary of the small Indian mongoose collected during February 2013 showed 3 Graafian follicles, indicating the state of preovulation (Figure 3A). Primary and secondary follicles were also present, representing normal ovarian cyclic growth. Light microscopic section of an ovarian tissue sample of a small Indian mongoose female collected during March 2013 showed events of the early gestation period (Figure 3B), with the corpus luteum being of moderate size and reddish yellow, and the antrum being a convoluted structure rather than being complete. The ovarian tissue section taken during April 2013 showed events of the late gestation period of the species, whereby corpora lutea were seen as the most prominent structures gathered along one side of the ovary at approximately the fifth week of pregnancy; the corpora lutea were observed to be fully enlarged (Figure 3C).
One of the light microscopic sections of the ovary in June 2013 indicated the lactation phase of the species,
containing no corpora lutea or ripe follicles (Figure 3D). Physical examination of the female mongooses of the same period showed that their mammary glands were heavy, indicating considerable glandular tissue.3.5. Length of gestation periodThe mating of the species was observed in the field during February, March, and April 2013 at different sampling sites. It was followed by the trapping of pregnant females during April, May, and June 2013. However, in the middle of June 2013, trapped females were found to be in the lactating state. Mating of mongooses was recorded on 6 and 7 April 2013, while their pups were observed for the first time on 16 June 2013. This indicates that pups had been born 21 days before, being altricial, most probably on 30 May 2013. By calculating the days back, the length of the gestation period is approximately 50 days. 3.6. Litter sizeMean litter size estimated by using data on visual observations was 2.83 ± 0.14 (Table 3). Results of counting placental scars showed that 12 females had a total of 36 placental scars, giving a litter size of 3 ± 0.24 per female (Figure 4). For embryo counts, 5 pregnant females were dissected and found to have a total of 16 embryos, with a mean litter size of 3.2 ± 0.37 (Table 3; Figure 4). A total of 36 pairs of mongooses observed in the field were found accompanying a total of 102 young ones (Figure 4).
Table 2. Monthly details of live-trapped male and female mongooses from different sampling sites to determine sex ratios (M: F) in the populations.
Total 36 couples 102 36 16Mean ± SE 2.83 ± 0.14 3 ± 0.24 3.2 ± 0.37
*In the column “No. of parents seen”, the numbers 1, 2, 3, etc. denote the parents, e.g., in the month of June 2012, a total of 5 couples were observed along with their 16 young ones.
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3.7. Statistical analysisNonparametric statistics were applied (Mann–Whitney U test) to check differences of medians in body weights as well as hormonal concentrations of estradiol, progesterone, FSH, and LH between the breeding and nonbreeding months of the mongoose species in the study area. The
results showed significant differences in body weights of female mongooses during breeding and nonbreeding months (U = 5.000; P = 0.05), while nonsignificant differences were found in estradiol (U = 24.000; P = 0.330), progesterone (U = 23.500; P = 0.371), FSH (U = 31.000; P = 0.35), and LH concentrations (U = 22.000; P = 0.516).
Figure 1. Levels of estradiol and progesterone in plasma samples of small Indian mongoose females (Herpestes javanicus) trapped on the Potohar Plateau.
Figure 2. Levels (mIU/mL) of follicle stimulating hormone (FSH) and luteinizing hormone (LH) in plasma samples of small Indian mongoose females (Herpestes javanicus) trapped on the Potohar Plateau. LH levels show 2 peaks (1 in September 2012 and 1 in March 2013).
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4. DiscussionSince males remain fertile throughout the year, the boundaries of the breeding season in mongooses are determined by the females (Pearson and Baldwin, 1953). Hormones, which are responsible for reproductive success, are indicators of the reproductive status of an individual, a population, or even a species (Brown and Wildt, 1997). In this context, a variety of environmental factors may play important roles in the regulation of seasonal breeding, including photoperiod, humidity, and temperature (Bronson and Heideman, 1990). Changes in photoperiod provide a cue for generating seasonal hormone fluctuations in mammals (Reiter, 1980). The reproductive system is triggered off or shut down when the photoperiod attains a certain critical day length (Saunders, 1977).
Most of the studies on reproductive physiology of small Indian mongooses so far have been conducted in regions where the species was introduced, such as on various islands like those of Fiji (Gorman, 1976), Grenada (Nellis and Everard, 1983), Hawaii (Hoffmann et al., 1984), and Okinawa (Ogura et al., 2001). Results of the current study show the breeding pattern of the small Indian mongoose in its native range. Earlier published studies cited above indicate that the small Indian mongoose breeds twice a year; females were found pregnant from August through February, with the last pregnant female found in February, unlikely on Grenada Island, where there was a 10-month breeding season (Nellis and Everard, 1983), with a gestation period of approximately 46–49 days. Similarly, Nellis (1989) reported a gestation period of 49 days, while
Figure 3. Light microscopic (hematoxylin and eosin stained) sections (40×) of the ovaries of female small Indian mongoose (Herpestes javanicus) from the Potohar Plateau, Pakistan: A) showing 3 Graafian follicles indicative of the state of preovulation during February 2013; B) events of early gestation period during March 2013, corpus luteum of moderate size and reddish yellow, antrum being a bit convoluted in structure rather than being complete; C) events of late gestation period during April 2013, whereby corpora lutea are seen as the most prominent structures; D) showing lactation phase of the species with no corpora lutea or ripe follicles during June 2013. (*P.F.: primary follicle; S.F.: secondary follicle; C.L.: corpus luteum; G.F.: Graafian follicle; Pr. F.: primordial follicle).
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Hoffmann et al. (1984) found it to be 50 days, with most of the pregnant females observed in February–September and lactating females observed in March through October. In the current study, pregnant females were found from April until June, with a gestation period of approximately 50 days. In addition, a low percentage of females (16%) were found pregnant, whereas Gorman (1976) reported high proportions of pregnant females on Fiji Island.
The male:female ratio in the present study seems to be more female-biased, indicating greater numbers of females than males, with a sex ratio of 0.67 males per female (n = 52). In contrast, Warren (1999) reported a male to female ratio on the island of Hawaii of 2.38 (n = 327) and on O’ahu of 2.44 (n = 921). Gorman (1979) showed on Fiji Island a male to female ratio of 1.51 (n = 83), while Nellis and Everard (1983) reported on Grenada a male to female
Figure 4. A) Foot prints of small Indian mongoose established around its burrow, B) Especially designed mesh trap for live capturing of the species, C) Placental Scars, D) Developing embryos inside the uteri of female mongoose exposed after dis-section, E) A vigilant mongoose, F) Small Indian mongoose and her pups caught in a live trap
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ratio of 2.80 (n = 1740) and on Trinidad a ratio of 1.18 (n = 207). All of these earlier reported studies show higher numbers of males in the populations of the small Indian mongoose, but in our study, under local conditions, the numbers of males have been lower than those of females, making the sex ratio more female-biased. This could be due to low success in capturing males in the study area.
During reproductive events, changes in physiology and behavior of the animal are mainly driven by varying sex hormone concentrations (Senger, 2003). Estrogen and progesterone levels in females provide information on basic reproductive parameters, such as cycle and length of gestation period, and this in turn provides insights into the physiological mechanisms causing reproductive seasonality (Ziegler et al., 2000) and hormone–behavior interactions, making clear the proximate mechanisms in the reproductive strategies of the females (Brockman and Whitten, 1996; Heistermann et al., 2001). In the current study, elevated concentrations of estradiol and progesterone from February until May 2013 compared to the rest of the months are indicative of the reproductive activity of the species. Two LH peaks have been observed, indicating ovulation (one during March and the other during September); this shows that the Potohar Plateau population of the small Indian mongoose may breed twice a year. De Magalhaes and Costa (2009) had earlier reported that small Indian mongoose breeds twice or 3 times a year, breeding being mostly correlated with food abundance. Studies on Okinawa Island (Ogura et al., 2001) and the island Viti Levu in Fiji (Gorman, 1976) have shown a single reproductive peak period (period with high ratio of pregnancy) in captured female mongooses. In contrast, 2 distinct peaks have been reported in Hawaii (Pearson and Baldwin, 1953), Puerto Rico (Pimentel, 1955), and St. Croix (Nellis and Everard, 1983); in Grenada, 3 distinct peaks were observed by Nellis and Everard (1983). In the areas where 2 or 3 distinct reproductive peaks were observed, there was an interval of 3 to 4 months between reproductive peaks, and females were able to reproduce 2 or 3 times a year. Pearson and Baldwin (1953) reported that on Hawaii the male mongoose is reproductively active from February to August and quiescent from September to December.
In this study, Graafian follicles were observed inside the ovary during February, indicating the preovulatory stage, while the presence of a moderate-sized corpus luteum during March and a large corpus luteum during April 2013 indicates early and late gestation periods. In June, no corpora lutea were seen inside ovaries, but the females
had considerable glandular tissue in the mammary glands, indicative of the lactation phase. Thus, pregnant females were observed during March and April and lactating females were observed during June. Earlier studies on island populations of the small Indian mongoose have reported pregnant females from August to late February in Fiji (Gorman, 1976), and from February to September in Hawaii (Pearson and Baldwin, 1953) and the US Virgin Islands, whereas the female mongooses on Grenada had a breeding season of 10 months (Nellis and Everard, 1983).
In the present study, body weights of the females during March, April, and May were generally heavier than in other months. In Herpestes auropunctatus of Hawaii, Hoffmann et al. (1984) reported no significant change in body weight during gestation and lactation conditions, but the weights of anterior pituitary, adrenal, ovarian, and uterine tissue were significantly reduced during the nonbreeding season.
Average litter size recorded during our study was approximately 3; visual observations of young ones accompanying their parents indicated a litter size of 2.83 ± 0.14, while counts of placental scars were 3 ± 0.24 with no signs of a second pregnancy during the same year. However, at Amami-oshima Island, Japan, a female trapped together with her pups showed a second early pregnancy during the same season (Abe et al., 2006). On the basis of placental scar counts, litter sizes of 5 placental scars have also have been recorded (Pearson and Baldwin, 1953; Gorman, 1976; Nellis and Everard, 1983; Coblentz and Coblentz, 1985); however, Abe et al. (2006) at Amami-oshima Island, Japan reported a litter size by both placental scars and embryo counts of 2.9. The litter size during this study by counts of developing embryos inside females was recorded as 3.2 ± 0.37 (16 embryos in 5 females; range: 2–4 embryos/female). Gorman (1976) found 1.8 ± 0.35 developing embryos in pregnant females (range: 1–4 embryos/female).
Lower litter size determined by visual observation of pups accompanying their parents as compared to the other 2 methods (counts of placental scars and developing embryos) perhaps indicates embryo abortion or death of newborns at early stages, or our limits in finding pups.
In conclusion, the occurrence of 2 peaks for LH (one in March and the other in September), along with the histological evidence of the changes occurring in the ovaries during the current study, indicates that the small Indian mongoose breeds twice a year in its native range of the Potohar Plateau. The gestation period is about 50 days and the average litter size is approximately 3 pups per female.
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